Biopolym. Cell. 1999; 15(4):262-274.
http://dx.doi.org/10.7124/bc.000523
Reviews
Does nitric oxide regulate the tumor necrosis factor signal transduction?
1Obolenskaya M. Yu., 1Samoilenko A. A.
  1. Institute of Molecular Biology and Genetics, NAS of Ukraine
    150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

This contribution is focused on the potential role of the nitric oxide in the perception and the intracellular transduction of tumor necrosis factor (TNF) signal. The data about concerted activities of TNF and nitric oxide in different physiological and pathophy-siological processes are presented. Particular attention is paid to the structural peculiarities of TNF intercellular messengers that provide the possible interaction of nitric oxide with these messengers. On the basis of conducted analysis and the existing data about nitric oxide interaction with some intercellular messengers of TNF signal transduction it is suggested that nitric oxide plays a definite role in manifestations of multiple TNF functions.
Full text: (PDF, in Ukrainian)

References

[1] Goeddel DV, Aggarwal BB, Gray PW, Leung DW, Nedwin GE, Palladino MA, Patton JS, Pennica D, Shepard HM, Sugarman BJ, et al. Tumor necrosis factors: gene structure and biological activities. Cold Spring Harb Symp Quant Biol. 1986;51 Pt 1:597-609.
[2] Beutler B, Cerami A. Tumor necrosis, cachexia, shock, and inflammation: a common mediator. Annu Rev Biochem. 1988;57:505-18.
[3] Fiers W. Tumor necrosis factor. Characterization at the molecular, cellular and in vivo level. FEBS Lett. 1991;285(2):199-212.
[4] Kroenke M, Schuetze S, Scheurich P, Pfizenmaier K. TNF transduction and TNF-responsive genes. Tumor Necrosis Factors: Structure, Function, and Mechanism of Action, Eds B. B. Aggarwal, J. Vilcek-New York; Basel; Hong Kong: Marcel Dekker Inc 1991 pp. 189-216.
[5] Beck G, Habicht GS. Primitive cytokines: harbingers of vertebrate defense. Immunol Today. 1991;12(6):180-3.
[6] Radomski MW, Martin JF, Moncada S. Synthesis of nitric oxide by the haemocytes of the American horseshoe crab (Limulus polyphemus). Phil. Trans. R. Soc. Lond., 1991;334(1269):129-133.
[7] Henry Y, Ducrocq C, Drapier JC, Servent D, Pellat C, Guissani A. Nitric oxide, a biological effector. Electron paramagnetic resonance detection of nitrosyl-iron-protein complexes in whole cells. Eur Biophys J. 1991;20(1):1-15.
[8] Henry Y, Lepoivre M, Drapier JC, Ducrocq C, Boucher JL, Guissani A. EPR characterization of molecular targets for NO in mammalian cells and organelles. FASEB J. 1993;7(12):1124-34.
[9] Moncada S, Palmer RM, Higgs EA. Nitric oxide: physiology, pathophysiology, and pharmacology. Pharmacol Rev. 1991;43(2):109-42.
[10] Kroncke KD, Fehsel K, Kolb-Bachofen V. Nitric oxide: cytotoxicity versus cytoprotection - how, why, when, and where? Nitric Oxide. 1997;1(2):107-20.
[11] Nathan C. Nitric oxide as a secretory product of mammalian cells. FASEB J. 1992;6(12):3051-64.
[12] Stamler JS, Simon DI, Osborne JA, Mullins ME, Jaraki O, Michel T, Singel DJ, Loscalzo J. S-nitrosylation of proteins with nitric oxide: synthesis and characterization of biologically active compounds. Proc Natl Acad Sci U S A. 1992;89(1):444-8.
[13] Stamler JS. Redox signaling: nitrosylation and related target interactions of nitric oxide. Cell. 1994;78(6):931-6.
[14] Marletta MA, Yoon PS, Iyengar R, Leaf CD, Wishnok JS. Macrophage oxidation of L-arginine to nitrite and nitrate: nitric oxide is an intermediate. Biochemistry. 1988;27(24):8706-11.
[15] Marletta MA. Nitric oxide synthase: aspects concerning structure and catalysis. Cell. 1994;78(6):927-30.
[16] Billiar TR, Curran RD, Stuehr DJ, West MA, Bentz BG, Simmons RL. An L-arginine-dependent mechanism mediates Kupffer cell inhibition of hepatocyte protein synthesis in vitro. J Exp Med. 1989;169(4):1467-72.
[17] Stadler J, Trockfeld J, Schmalix WA, Brill T, Siewert JR, Greim H, Doehmer J. Inhibition of cytochromes P4501A by nitric oxide. Proc Natl Acad Sci U S A. 1994;91(9):3559-63.
[18] Curran RD, Billiar TR, Stuehr DJ, Ochoa JB, Harbrecht BG, Flint SG, Simmons RL. Multiple cytokines are required to induce hepatocyte nitric oxide production and inhibit total protein synthesis. Ann Surg. 1990;212(4):462-9
[19] Eigler A, Sinha B, Endres S. Nitric oxide-releasing agents enhance cytokine-induced tumor necrosis factor synthesis in human mononuclear cells. Biochem Biophys Res Commun. 1993;196(1):494-501.
[20] Old LJ. Tumor necrosis factor (TNF). Science. 1985;230(4726):630-2.
[21] Pohlman TH, Harlan JM. Human endothelial cell response to lipopolysaccharide, interleukin-1, and tumor necrosis factor is regulated by protein synthesis. Cell Immunol. 1989;119(1):41-52.
[22] Beyaert R, Fiers W. Molecular mechanisms of tumor necrosis factor-induced cytotoxicity. What we do understand and what we do not. FEBS Lett. 1994;340(1-2):9-16.
[23] Muzio M, Chinnaiyan AM, Kischkel FC, O'Rourke K, Shevchenko A, Ni J, Scaffidi C, Bretz JD, Zhang M, Gentz R, Mann M, Krammer PH, Peter ME, Dixit VM. FLICE, a novel FADD-homologous ICE/CED-3-like protease, is recruited to the CD95 (Fas/APO-1) death--inducing signaling complex. Cell. 1996;85(6):817-27.
[24] Hibbs JB Jr, Taintor RR, Vavrin Z, Rachlin EM. Nitric oxide: a cytotoxic activated macrophage effector molecule. Biochem Biophys Res Commun. 1988;157(1):87-94.
[25] Estrada C, Gomez C, Martin C, Moncada S, Gonzalez C. Nitric oxide mediates tumor necrosis factor-alpha cytotoxicity in endothelial cells. Biochem Biophys Res Commun. 1992;186(1):475-82.
[26] Larrick JW, Wright SC. Cytotoxic mechanism of tumor necrosis factor-alpha. FASEB J. 1990;4(14):3215-23.
[27] Camussi G, Albano E, Tetta C, Bussolino F. The molecular action of tumor necrosis factor-alpha. Eur J Biochem. 1991;202(1):3-14.
[28] Heller RA1, Kronke M. Tumor necrosis factor receptor-mediated signaling pathways. J Cell Biol. 1994;126(1):5-9.
[29] Remington JS, Merigan TC. Resistance to virus challenge in mice infected with protozoa or bacteria. Proc Soc Exp Biol Med. 1969;131(4):1184-8.
[30] Aono K, Isobe K, Nakashima I, Kondo S, Miyachi M, Nimura Y. Kupffer cells cytotoxicity against hepatoma cells is related to nitric oxide. Biochem Biophys Res Commun. 1994;201(3):1175-81.
[31] Ioannidis I1, de Groot H. Cytotoxicity of nitric oxide in Fu5 rat hepatoma cells: evidence for co-operative action with hydrogen peroxide. Biochem J. 1993;296 ( Pt 2):341-5.
[32] Decker, K. Basic mechanisms of the inflammatory response (1991) 42 Colloquim Mosbach. Molecular Aspects of Inflammation,Berlin; Heidelberg: Springer pp. 1-23.
[33] Freudenberg MA, Freudenberg N, Galanos C. Time course of cellular distribution of endotoxin in liver, lungs and kidneys of rats. Br J Exp Pathol. 1982;63(1):56-65.
[34] Decker K. Biologically active products of stimulated liver macrophages (Kupffer cells). Eur J Biochem. 1990;192(2):245-61.
[35] Pfeffer K, Matsuyama T, Kundig TM, Wakeham A, Kishihara K, Shahinian A, Wiegmann K, Ohashi PS, Kranke M, Mak TW. Mice deficient for the 55 kd tumor necrosis factor receptor are resistant to endotoxic shock, yet succumb to L. monocytogenes infection. Cell. 1993;73(3):457-67.
[36] Wagner DA, Young VR, Tannenbaum SR. Mammalian nitrate biosynthesis: incorporation of 15NH3 into nitrate is enhanced by endotoxin treatment. Proc Natl Acad Sci U S A. 1983;80(14):4518-21.
[37] Palmer RM, Ferrige AG, Moncada S. Nitric oxide release accounts for the biological activity of endothelium-derived relaxing factor. Nature. 1987 Jun 11-17;327(6122):524-6.
[38] Mulligan MS, Hevel JM, Marletta MA, Ward PA. Tissue injury caused by deposition of immune complexes is L-arginine dependent. Proc Natl Acad Sci U S A. 1991;88(14):6338-42.
[39] Chander CL, Moore AR, Desa FM, Howat DW, Willoughby DA. Anti-inflammatory effects of endothelin-1. J Cardiovasc Pharmacol. 1989;13 Suppl 5:S218-9.
[40] Kilbourn RG, Jubran A, Gross SS, Griffith OW, Levi R, Adams J, Lodato RF. Reversal of endotoxin-mediated shock by NG-methyl-L-arginine, an inhibitor of nitric oxide synthesis. Biochem Biophys Res Commun. 1990;172(3):1132-8.
[41] Veihelmann A, Brill T, Blobner M, Scheller I, Mayer B, Prölls M, Himpel S, Stadler J. Inhibition of nitric oxide synthesis improves detoxication in inflammatory liver dysfunction in vivo. Am J Physiol. 1997;273(2 Pt 1):G530-6.
[42] Harbrecht BG, Stadler J, Demetris AJ, Simmons RL, Billiar TR. Nitric oxide and prostaglandins interact to prevent hepatic damage during murine endotoxemia. Am J Physiol. 1994;266(6 Pt 1):G1004-10.
[43] Billiar TR, Curran RD, Harbrecht BG, Stuehr DJ, Demetris AJ, Simmons RL. Modulation of nitrogen oxide synthesis in vivo: NG-monomethyl-L-arginine inhibits endotoxin-induced nitrate/nitrate biosynthesis while promoting hepatic damage. J Leukoc Biol. 1990;48(6):565-9.
[44] Hutcheson IR, Whittle BJ, Boughton-Smith NK. Role of nitric oxide in maintaining vascular integrity in endotoxin-induced acute intestinal damage in the rat. Br J Pharmacol. 1990;101(4):815-20.
[45] Malyshev IYu, Malugin AV, Golubeva LYu, Zenina TA, Manukhina EB, Mikoyan VD, Vanin AF. Nitric oxide donor induces HSP70 accumulation in the heart and in cultured cells. FEBS Lett. 1996;391(1-2):21-3.
[46] Kim YM, de Vera ME, Watkins SC, Billiar TR. Nitric oxide protects cultured rat hepatocytes from tumor necrosis factor-alpha-induced apoptosis by inducing heat shock protein 70 expression. J Biol Chem. 1997;272(2):1402-11.
[47] Vilcek, J., Palombella, V.J. TNF as a Growth Factor (1991) Tumor necrosis factor: Structure, Function and Mechanism of Action, Eds B. B. Aggarwal, J. Vilcek.-New York; Basel; Hong Kong: Marcel Dekker Inc pp. 269-286.
[48] Brenner DA, O'Hara M, Angel P, Chojkier M, Karin M. Prolonged activation of jun and collagenase genes by tumour necrosis factor-alpha. Nature. 1989;337(6208):661-3.
[49] Lin JX, Vilcek J. Tumor necrosis factor and interleukin-1 cause a rapid and transient stimulation of c-fos and c-myc mRNA levels in human fibroblasts. J Biol Chem. 1987;262(25):11908-11.
[50] Kalthoff H, Roeder C, Brockhaus M, Thiele HG, Schmiegel W. Tumor necrosis factor (TNF) up-regulates the expression of p75 but not p55 TNF receptors, and both receptors mediate, independently of each other, up-regulation of transforming growth factor alpha and epidermal growth factor receptor mRNA. J Biol Chem. 1993;268(4):2762-6.
[51] Tamura M, Arakaki N, Tsubouchi H, Takada H, Daikuhara Y. Enhancement of human hepatocyte growth factor production by interleukin-1 alpha and -1 beta and tumor necrosis factor-alpha by fibroblasts in culture. J Biol Chem. 1993;268(11):8140-5.
[52] Obolenskaya MYu. Cytokines and liver regeneration. EOS Rivista di Immunologia ed Immunofarmacologia, 1997; 17(2):51-58.
[53] Obolenskaya MYu, Bernauer H, Tran-Thi TA, Decker K. Levels of rna for TNF-a and receptors during the prereplicative period of liver regeneration. Biopolym. Cell, 1994;10(5):68-77
[54] Yamada Y, Kirillova I, Peschon JJ, Fausto N. Initiation of liver growth by tumor necrosis factor: deficient liver regeneration in mice lacking type I tumor necrosis factor receptor. Proc Natl Acad Sci U S A. 1997;94(4):1441-6.
[55] Obolenskaya MYu, Vanin AF, Mordvintcev PI, Mülsch A, Decker K. Epr evidence of nitric oxide production by the regenerating rat liver. Biochem Biophys Res Commun. 1994;202(1):571-6.
[56] Obolenskaya M, Schulze-Specking A, Plaumann B, Frenzer K, Freudenberg N, Decker K. Nitric oxide production by cells isolated from regenerating rat liver. Biochem Biophys Res Commun. 1994;204(3):1305-11.
[57] Bauche F, Stephan JP, Touzalin AM, Jegou B. In vitro regulation of an inducible-type NO synthase in the rat seminiferous tubule cells. Biol Reprod. 1998;58(2):431-8.
[58] Kuemmerle JF. Synergistic regulation of NOS II expression by IL-1 beta and TNF-alpha in cultured rat colonic smooth muscle cells. Am J Physiol. 1998;274(1 Pt 1):G178-85.
[59] Saura M, Lopez S, Rodriguez Puyol M, Rodriguez Puyol D, Lamas S. Regulation of inducible nitric oxide synthase expression in rat mesangial cells and isolated glomeruli. Kidney Int. 1995;47(2):500-9.
[60] Worrall NK, Chang K, LeJeune WS, Misko TP, Sullivan PM, Ferguson TB Jr, Williamson JR. TNF-alpha causes reversible in vivo systemic vascular barrier dysfunction via NO-dependent and -independent mechanisms. Am J Physiol. 1997;273(6 Pt 2):H2565-74.
[61] Uchida Y, Tsukahara F, Ohba K, Ogawa A, Irie K, Fujii E, Yoshimoto T, Yoshioka T, Muraki T. Nitric oxide mediates down regulation of lipoprotein lipase activity induced by tumor necrosis factor-alpha in brown adipocytes. Eur J Pharmacol. 1997;335(2-3):235-43.
[62] Irie K, Tsukahara F, Fujii E, Uchida Y, Yoshioka T, He WR, Shitashige M, Murota S, Muraki T. Cationic amino acid transporter-2 mRNA induction by tumor necrosis factor-alpha in vascular endothelial cells. Eur J Pharmacol. 1997;339(2-3):289-93.
[63] Van Dervort AL, Yan L, Madara PJ, Cobb JP, Wesley RA, Corriveau CC, Tropea MM, Danner RL. Nitric oxide regulates endotoxin-induced TNF-alpha production by human neutrophils. J Immunol. 1994;152(8):4102-9.
[64] Magrinat G, Mason SN, Shami PJ, Weinberg JB. Nitric oxide modulation of human leukemia cell differentiation and gene expression. Blood. 1992;80(8):1880-4.
[65] Eigler A, Moeller J, Endres S. Exogenous and endogenous nitric oxide attenuates tumor necrosis factor synthesis in the murine macrophage cell line RAW 264.7. J Immunol. 1995;154(8):4048-54.
[66] Eck MJ, Sprang SR. The structure of tumor necrosis factor-alpha at 2.6 A resolution. Implications for receptor binding. J Biol Chem. 1989;264(29):17595-605.
[67] Banner DW, D'Arcy A, Janes W, Gentz R, Schoenfeld HJ, Broger C, Loetscher H, Lesslauer W. Crystal structure of the soluble human 55 kd TNF receptor-human TNF beta complex: implications for TNF receptor activation. Cell. 1993;73(3):431-45.
[68] Bazan JF. Emerging families of cytokines and receptors. Curr Biol. 1993;3(9):603-6.
[69] Vandenabeele P, Declercq W, Beyaert R, Fiers W. Two tumour necrosis factor receptors: structure and function. Trends Cell Biol. 1995;5(10):392-9.
[70] Porteu F, Hieblot C. Tumor necrosis factor induces a selective shedding of its p75 receptor from human neutrophils. J Biol Chem. 1994;269(4):2834-40.
[71] Mosselmans R, Hepburn A, Dumont JE, Fiers W, Galand P. Endocytic pathway of recombinant murine tumor necrosis factor in L-929 cells. J Immunol. 1988;141(9):3096-100.
[72] D'Arcy A, Banner DW, Janes W, Winkler FK, Loetscher H, Schönfeld HJ, Zulauf M, Gentz R, Lesslauer W. Crystallization and preliminary crystallographic analysis of a TNF-beta-55 kDa TNF receptor complex. J Mol Biol. 1993;229(2):555-7.
[73] Tartaglia LA, Ayres TM, Wong GH, Goeddel DV. A novel domain within the 55 kd TNF receptor signals cell death. Cell. 1993;74(5):845-53.
[74] Boldin MP, Mett IL, Varfolomeev EE, Chumakov I, Shemer-Avni Y, Camonis JH, Wallach D. Self-association of the "death domains" of the p55 tumor necrosis factor (TNF) receptor and Fas/APO1 prompts signaling for TNF and Fas/APO1 effects. J Biol Chem. 1995;270(1):387-91.
[75] Song HY, Dunbar JD, Donner DB. Aggregation of the intracellular domain of the type 1 tumor necrosis factor receptor defined by the two-hybrid system. J Biol Chem. 1994;269(36):22492-5.
[76] Wiegmann K, Schutze S, Machleidt T, Witte D, Kronke M. Functional dichotomy of neutral and acidic sphingomyelinases in tumor necrosis factor signaling. Cell. 1994;78(6):1005-15.
[77] Belka C, Wiegmann K, Adam D, Holland R, Neuloh M, Herrmann F, Krönke M, Brach MA. Tumor necrosis factor (TNF)-alpha activates c-raf-1 kinase via the p55 TNF receptor engaging neutral sphingomyelinase. EMBO J. 1995;14(6):1156-65.
[78] Adam D, Wiegmann K, Adam-Klages S, Ruff A, Krönke M. A novel cytoplasmic domain of the p55 tumor necrosis factor receptor initiates the neutral sphingomyelinase pathway. J Biol Chem. 1996;271(24):14617-22.
[79] Rothe M, Wong SC, Henzel WJ, Goeddel DV. A novel family of putative signal transducers associated with the cytoplasmic domain of the 75 kDa tumor necrosis factor receptor. Cell. 1994;78(4):681-92.
[80] Hsu H, Xiong J, Goeddel DV. The TNF receptor 1-associated protein TRADD signals cell death and NF-kappa B activation. Cell. 1995;81(4):495-504.
[81] Baker SJ, Reddy EP. Transducers of life and death: TNF receptor superfamily and associated proteins. Oncogene. 1996;12(1):1-9.
[82] Liu ZG, Hsu H, Goeddel DV, Karin M. Dissection of TNF receptor 1 effector functions: JNK activation is not linked to apoptosis while NF-kappaB activation prevents cell death. Cell. 1996;87(3):565-76.
[83] Yuan J. Transducing signals of life and death. Curr Opin Cell Biol. 1997;9(2):247-51.
[84] Chinnaiyan AM, O'Rourke K, Tewari M, Dixit VM. FADD, a novel death domain-containing protein, interacts with the death domain of Fas and initiates apoptosis. Cell. 1995;81(4):505-12.
[85] Boldin MP, Varfolomeev EE, Pancer Z, Mett IL, Camonis JH, Wallach D. A novel protein that interacts with the death domain of Fas/APO1 contains a sequence motif related to the death domain. J Biol Chem. 1995;270(14):7795-8.
[86] Claudio E, Segade F, Wrobel K, Ramos S, Bravo R, Lazo PS. Molecular mechanisms of TNFalpha cytotoxicity: activation of NF-kappaB and nuclear translocation. Exp Cell Res. 1996;224(1):63-71.
[87] Adam-Klages S, Adam D, Wiegmann K, Struve S, Kolanus W, Schneider-Mergener J, Kronke M. FAN, a novel WD-repeat protein, couples the p55 TNF-receptor to neutral sphingomyelinase. Cell. 1996;86(6):937-47.
[88] Hsu H, Shu HB, Pan MG, Goeddel DV. TRADD-TRAF2 and TRADD-FADD interactions define two distinct TNF receptor 1 signal transduction pathways. Cell. 1996;84(2):299-308.
[89] Takeuchi M, Rothe M, Goeddel DV. Anatomy of TRAF2. Distinct domains for nuclear factor-kappaB activation and association with tumor necrosis factor signaling proteins. J Biol Chem. 1996;271(33):19935-42.
[90] Lovering R, Hanson IM, Borden KL, Martin S, O'Reilly NJ, Evan GI, Rahman D, Pappin DJ, Trowsdale J, Freemont PS. Identification and preliminary characterization of a protein motif related to the zinc finger. Proc Natl Acad Sci U S A. 1993;90(6):2112-6.
[91] Miller J, McLachlan AD, Klug A. Repetitive zinc-binding domains in the protein transcription factor IIIA from Xenopus oocytes. EMBO J. 1985;4(6):1609-14.
[92] Berg JM. Zinc fingers and other metal-binding domains. Elements for interactions between macromolecules. J Biol Chem. 1990;265(12):6513-6.
[93] Pellegrini S, Dusanter-Fourt I. The structure, regulation and function of the Janus kinases (JAKs) and the signal transducers and activators of transcription (STATs). Eur J Biochem. 1997;248(3):615-33.
[94] Boldin MP, Goncharov TM, Goltsev YV, Wallach D. Involvement of MACH, a novel MORT1/FADD-interacting protease, in Fas/APO-1- and TNF receptor-induced cell death. Cell. 1996;85(6):803-15.
[95] Schwandner R, Wiegmann K, Bernardo K, Kreder D, Kronke M. TNF receptor death domain-associated proteins TRADD and FADD signal activation of acid sphingomyelinase. J Biol Chem. 1998;273(10):5916-22.
[96] Mathias S, Dressler KA, Kolesnick RN. Characterization of a ceramide-activated protein kinase: stimulation by tumor necrosis factor alpha. Proc Natl Acad Sci U S A. 1991;88(22):10009-13.
[97] Dobrowsky RT, Kamibayashi C, Mumby MC, Hannun YA. Ceramide activates heterotrimeric protein phosphatase 2A. J Biol Chem. 1993;268(21):15523-30.
[98] Uren AG, Pakusch M, Hawkins CJ, Puls KL, Vaux DL. Cloning and expression of apoptosis inhibitory protein homologs that function to inhibit apoptosis and/or bind tumor necrosis factor receptor-associated factors. Proc Natl Acad Sci U S A. 1996;93(10):4974-8.
[99] Mosialos G, Birkenbach M, Yalamanchili R, VanArsdale T, Ware C, Kieff E. The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell. 1995;80(3):389-99.
[100] Clem RJ, Fechheimer M, Miller LK. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science. 1991;254(5036):1388-90.
[101] Shu HB, Halpin DR, Goeddel DV. Casper is a FADD- and caspase-related inducer of apoptosis. Immunity. 1997;6(6):751-63.
[102] Srinivasula SM, Ahmad M, Ottilie S, Bullrich F, Banks S, Wang Y, Fernandes-Alnemri T, Croce CM, Litwack G, Tomaselli KJ, Armstrong RC, Alnemri ES. FLAME-1, a novel FADD-like anti-apoptotic molecule that regulates Fas/TNFR1-induced apoptosis. J Biol Chem. 1997;272(30):18542-5.
[103] Song HY, Rothe M, Goeddel DV. The tumor necrosis factor-inducible zinc finger protein A20 interacts with TRAF1/TRAF2 and inhibits NF-kappaB activation. Proc Natl Acad Sci U S A. 1996;93(13):6721-5.
[104] Cheng G, Baltimore D. TANK, a co-inducer with TRAF2 of TNF- and CD 40L-mediated NF-kappaB activation. Genes Dev. 1996;10(8):963-73.
[105] Quaroni L, Reglinski J, Wolf R, Smith WE. Interaction of nitrogen monoxide with cytochrome P-450 monitored by surface-enhanced resonance Raman scattering. Biochim Biophys Acta. 1996;1296(1):5-8.
[106] Estrada C, Gomez C, Martin-Nieto J, De Frutos T, Jimenez A, Villalobo A. Nitric oxide reversibly inhibits the epidermal growth factor receptor tyrosine kinase. Biochem J. 1997;326(Pt 2):369-76.
[107] Mohr S, Stamler JS, Brune B. Posttranslational modification of glyceraldehyde-3-phosphate dehydrogenase by S-nitrosylation and subsequent NADH attachment. J Biol Chem. 1996;271(8):4209-14.
[108] Stamler JS, Simon DI, Jaraki O, Osborne JA, Francis S, Mullins M, Singel D, Loscalzo J. S-nitrosylation of tissue-type plasminogen activator confers vasodilatory and antiplatelet properties on the enzyme. Proc Natl Acad Sci U S A. 1992;89(17):8087-91.
[109] Lander HM, Ogiste JS, Pearce SF, Levi R, Novogrodsky A. Nitric oxide-stimulated guanine nucleotide exchange on p21ras. J Biol Chem. 1995;270(13):7017-20.
[110] Ignarro LJ. Biosynthesis and metabolism of endothelium-derived nitric oxide. Annu Rev Pharmacol Toxicol. 1990;30:535-60.
[111] Vanin AF, Malenkova IV, Serezhenkov VA. Iron catalyzes both decomposition and synthesis of S-nitrosothiols: optical and electron paramagnetic resonance studies. Nitric Oxide. 1997;1(3):191-203.
[112] Gopalakrishna R, Chen ZH, Gundimeda U. Nitric oxide and nitric oxide-generating agents induce a reversible inactivation of protein kinase C activity and phorbol ester binding. J Biol Chem. 1993;268(36):27180-5.
[113] Lei SZ, Pan ZH, Aggarwal SK, Chen HS, Hartman J, Sucher NJ, Lipton SA. Effect of nitric oxide production on the redox modulatory site of the NMDA receptor-channel complex. Neuron. 1992;8(6):1087-99.
[114] Caselli A, Camici G, Manao G, Moneti G, Pazzagli L, Cappugi G, Ramponi G. Nitric oxide causes inactivation of the low molecular weight phosphotyrosine protein phosphatase. J Biol Chem. 1994;269(40):24878-82.
[115] Huang RP, Adamson ED. Characterization of the DNA-binding properties of the early growth response-1 (Egr-1) transcription factor: evidence for modulation by a redox mechanism. DNA Cell Biol. 1993;12(3):265-73.
[116] Kroncke KD, Fehsel K, Schmidt T, Zenke FT, Dasting I, Wesener JR, Bettermann H, Breunig KD, Kolb-Bachofen V. Nitric oxide destroys zinc-sulfur clusters inducing zinc release from metallothionein and inhibition of the zinc finger-type yeast transcription activator LAC9. Biochem Biophys Res Commun. 1994;200(2):1105-10.
[117] Wink DA, Laval J. The Fpg protein, a DNA repair enzyme, is inhibited by the biomediator nitric oxide in vitro and in vivo. Carcinogenesis. 1994;15(10):2125-9.
[118] Kroncke KD, Kolb-Bachofen V. Detection of nitric oxide interaction with zinc finger proteins. Methods Enzymol. 1996;269:279-84.
[119] Aggarwal BB, Kohr WJ, Hass PE, Moffat B, Spencer SA, Henzel WJ, Bringman TS, Nedwin GE, Goeddel DV, Harkins RN. Human tumor necrosis factor. Production, purification, and characterization. J Biol Chem. 1985;260(4):2345-54.
[120] Kobayashi Y, Miyamoto D, Asada M, Obinata M, Osawa T. Cloning and expression of human lymphotoxin mRNA derived from a human T cell hybridoma. J Biochem. 1986;100(3):727-33.
[121] Dadlez M. Disulfide bonds in protein folding studies: friends or foes? Acta Biochim Pol. 1997;44(3):433-52.
[122] Darnay BG, Aggarwal BB. Inhibition of protein tyrosine phosphatases causes phosphorylation of tyrosine-331 in the p60 TNF receptor and inactivates the receptor-associated kinase. FEBS Lett. 1997;410(2-3):361-7.
[123] Uchida K, Morita T, Sato T, Ogura T, Yamashita R, Noguchi S, Suzuki H, Nyunoya H, Miwa M, Sugimura T. Nucleotide sequence of a full-length cDNA for human fibroblast poly(ADP-ribose) polymerase. Biochem Biophys Res Commun. 1987;148(2):617-22.
[124] Haendeler J, Weiland U, Zeiher AM, Dimmeler S. Effects of redox-related congeners of NO on apoptosis and caspase-3 activity. Nitric Oxide. 1997;1(4):282-93.
[125] Peunova N, Enikolopov G. Amplification of calcium-induced gene transcription by nitric oxide in neuronal cells. Nature. 1993;364(6436):450-3.
[126] Lander HM, Sehajpal PK, Novogrodsky A. Nitric oxide signaling: a possible role for G proteins. J Immunol. 1993;151(12):7182-7.
[127] Schreck R, Baeuerle PA. A role for oxygen radicals as second messengers. Trends Cell Biol. 1991;1(2-3):39-42.